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Patterns of muscle activity during different behaviors in chicks: implications for neural control

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Abstract

The large behavioral repertoire that spans the embryonic and postembryonic stages of development make chicks an ideal system for identifying patterns of muscle activity that are common to different behaviors and those that are behavior-specific. The main goal of this work was to identify the similar and dissimilar aspects of the recruitment patterns and the regulation of muscle activity during three distinct postembryonic behaviors: walking, swimming and airstepping. We identified two synergies that were common to each of these behaviors. The synergies were not disrupted by the absence of FT1 activity in airstepping. Within each synergy the recruitment time, recruitment order and duration of activity were not rigid, but varied according to the context-specific resistance that the leg encountered. Unlike the other muscles, FT2 activity was not recruited as part of the same synergy in each behavior. When weight-bearing contact with the substrate did not occur, as in swimming and airstepping, as well as in walking in chicks with deafferented legs, FT2 activity was not recruited as part of either synergy, but was recruited during the time between them. Although not identical, embryonic motility and hatching motor pattern both show the two synergies described for the postembryonic behaviors. Like the latter behaviors, the synergies tolerated the absence of activity from specific muscles. Thus, we suggest that the CNS produces different behaviors using many of the same muscles by organizing the patterned activity around two common synergies while permitting the different muscles that participate in a synergy to be modified in tandem or on an individual basis. Furthermore, the common synergies are established early during prenatal development in chicks.

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Abbreviations

aIF :

anterior iliofibularius

CF :

caudilioflexorius

CNS :

central nervous system

EMG :

electromyogram

FT :

femorotibialis

GL :

gastrocnemius lateralis

P1 :

protraction 1

P2 :

protraction 2

pIF :

posterior iliofibularis

R :

retraction

SA :

sartorius

TA :

tibialis anterior

pIF :

posterior iliofibularis

ms :

millisecond

References

  • Abraham GV, Loeb G (1985) The distal hindlimb musculature of the cat. Patterns of normal use. Exp Brain Res 58: 580–593

    Google Scholar 

  • American Veterinary Medicine Association (1993) Report of the AVMA panel on euthanasia. J Am Vet Med Assoc 202: 229–249

    Google Scholar 

  • Ayers JL, Clarac F (1978) Neuromuscular strategies underlying different behavioral acts in a multifunctional crustacean leg joint. J Comp Physiol 128: 81–94

    Google Scholar 

  • Ayers JL, Davis WJ (1977) Neural control of locomotion in the lobster, Homarus americanus. J Comp Physiol 115: 1–27

    Google Scholar 

  • Bässler U (1989) Muscle and reflex partitioning in insects? Behav Brain Sci 12: 646–647

    Google Scholar 

  • Bässler U, Wegner U (1983) Motor output of the denervated thoracic ventral nerve cord in the stick insect Carausius morosus. J Exp Biol 105: 127–145

    Google Scholar 

  • Bekoff A (1976) Ontogeny of leg motor output in the chick embryo: a neural analysis. Brain Res 106: 271–291

    Google Scholar 

  • Bekoff A (1986) Ontogeny of chicken motor behaviors: evidence for multi-use limb pattern generating circuitry. In: Grillner S, Stein PSG, Stuart DG, Forssberg H, Herman RM (eds) Neurobiology of vertebrate locomotion. Macmillian, Hampshire, England, pp 433–453

    Google Scholar 

  • Bekoff A (1988) Embryonic motor output and movement patterns: relationships to postnatal behavior. In: Smotherman WP, Robinson SR (eds) Behavior of the fetus. Telford Press New Jersey, pp 191–206

    Google Scholar 

  • Bekoff A, Kauer JA (1982) Neural control of hatching: role of neck position in turning on hatching leg movements in post-hatching chicks. J Comp Physiol 145: 497–504

    Google Scholar 

  • Bekoff A, Kauer JA (1984) Neural control of hatching: fate of the pattern generator for the leg movements of hatching in post-hatching chicks. J Neurosci 4: 2659–2666

    Google Scholar 

  • Bekoff A, Sabichi AL (1987) Sensory control of the initiation of hatching in chicks: effects of local anesthetic injected into the neck. Dev Psychobiol 20: 489–495

    Google Scholar 

  • Bekoff A, Nusbaum MP, Sabichi AL, Clifford M (1987) Neural control of limb coordination: comparison of hatching and walking motor output patterns in normal and deafferented chicks. J Neurosci 7: 2320–2330

    Google Scholar 

  • Bradley NS, Bekoff A (1990) Development of coordinated movement in chicks: I. Temporal analysis of hindlimb muscle synergies at embryonic days 9 and 10. Dev Psychobiol 23: 763–782

    Google Scholar 

  • Cazalets J-R, Nagy F, Moulins M (1990) Suppressive control of the crustacean pyloric network by a pair of identified interneurons. I. Modulation of the motor pattern. J Neurosci 10: 448–457

    CAS  PubMed  Google Scholar 

  • Cracraft J (1971) The functional morphology of the hind limb of the domestic pigeon, Columba livia. Bull Am Mus Nat Hist 144: 171–268

    Google Scholar 

  • Dickinson P, Mecsas C, Marder E (1990) Neuropeptide fusion of two motor-pattern generator circuits. Nature 344: 155–258

    Google Scholar 

  • Gatesy SM (1989) Archosaur neuromuscular and locomotor evolution. PhD thesis. Harvard University

  • Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12: 185–204

    Google Scholar 

  • Getting PA, Dekin MS (1985) A model system for integration within rhythmic motor systems. In: Selverston AI (ed) Model neural networks and behavior. Plenum, New York, pp 3–20

    Google Scholar 

  • Giuliani CA, Smith JL (1985) Development and characteristics of airstepping in chronic spinal cats. J Neurosci 5: 1276–1282

    Google Scholar 

  • Grillner S (1981) Control of locomotion in bipeds, tetrapods and fish. In: Brooks VB (ed) The Handbook of Physiology, section 1. The Nervous System, vol. II. Am Physiol Soc, Bethesda, Maryland, pp 1179–1236

    Google Scholar 

  • Grillner S, Wallén P (1985) Central pattern generators for locomotion, with special reference to vertebrates. Annu Rev Neurosci 8: 233–261

    Google Scholar 

  • Gruner JA, Altman J (1980) Swimming in the rat: analysis of locomotor performance in comparison to stepping. Exp Brain Res 40: 374–382

    Google Scholar 

  • Harris-Warrick RM, Johnson BR (1989) Motor pattern networks: flexible foundations for rhythmical pattern production. In:Crew TJ, Kelley DB (eds) Perspectives in neural systems and behavior. A.R. Liss, New York, pp 55–71

    Google Scholar 

  • Harris-Warrick RM, Marder E (1991) Modulation of neural networks for behavior. Annu Rev Neurosci 14: 39–57

    Article  CAS  PubMed  Google Scholar 

  • Hooper SL, Moulins M (1989) Switching of a neuron from one network to another by sensory-induced changes in membrane properties. Science 244: 1587–1589

    Google Scholar 

  • Hoy MG, Zernicke RF (1986) The role of intersegmental dynamics during rapid limb oscillations. J Biomech 19: 867–877

    Article  CAS  PubMed  Google Scholar 

  • Hoy MG, Zernicke RF, Smith JL (1985) Contrasting roles of inertial and muscle moments at the knee and ankle during paw-shake response. J Neurophysiol 54: 1282–1294

    Google Scholar 

  • Jacobson RD, Hollyday MA (1982) A behavioral and electromyographic study of walking in the chick. J Neurophysiol 48: 238–256

    Google Scholar 

  • Johnston RM, Bekoff AC (1992) Constrained and flexible features of rhythmical hindlimb movements in chicks: kinematic profiles of walking, swimming and airstepping. J Exp Biol 171: 43–66

    Google Scholar 

  • Keller C, Heiligenberg W (1989) From distributed sensory processing to discrete motor representations in the diencephalon of the electric fish, Eigenmannia. J Comp Physiol A 164: 565–576

    Google Scholar 

  • Koshland GF, Smith JL (1989) Mutable and immutable features of paw-shake responses after hindlimb deafferentation in the cat. J Neurophysiol 62: 162–173

    Google Scholar 

  • Landmesser LT, O'Donavan MJ (1984) Activation patterns of embryonic chick hindlimb muscles recorded in ovo and in an isolated spinal cord preparation. J Physiol 347: 189–204

    Google Scholar 

  • Lennard PR, Stein PSG (1977) Swimming movements elicited by electrical stimulation of turtle spinal cord. I. Low-spinal and intact preparations. J Neurophysiol 40: 768–778

    Google Scholar 

  • Levine RB, Weeks JC (1989) Reorganization of neural circuits and behavior during insect metamorphosis. In: Crew TJ, Kelley DB (eds) Perspectives in neural systems and behavior. A.R. Liss, New York, pp 195–228

    Google Scholar 

  • Machlis L, Dodd PWD, Fentress JC (1985) The pooling fallacy: problems arising when individuals contribute more than one observation to a data set. Z Tierpsychol 68: 201–214

    Google Scholar 

  • MacPherson JM (1991) How flexible are muscle synergies? In: Humphrey DR, Freund HJ (eds) Motor control: Concepts and issues. John Wiley, New York, pp 33–47

    Google Scholar 

  • Meyrand P, Simmers J (1992) An unstable brain for stable behaviors. In: Proceedings of the Third International Congress of Neuroethology. McGill University Press, Montreal, p 64

    Google Scholar 

  • Meyrand P, Simmers J, Moulins M (1991) Construction of a pattern-generating circuit with neurons of different networks. Nature 351: 60–63

    Article  CAS  PubMed  Google Scholar 

  • Mortin LI, Stein PSG (1989) Spinal cord segments containing key elements of the central pattern generators for three forms of scratch reflex in the turtle. J Neurosci 9: 2285–2296

    Google Scholar 

  • Pflüger H-J, Burrows M (1978) Locust use the same basic motor patterns in swimming as in jumping and in kicking. J Exp Biol 75: 81–93

    Google Scholar 

  • Pratt CA, Loeb GE (1991) Functional complex muscles of the cat hindlimb. I. Patterns of activation across sartorius. Exp Brain Res 85: 243–256

    Google Scholar 

  • Raikow RJ (1985) Locomotor system. In: King AS, McLelland J (eds) Form and function in birds, vol. 3. Academic Press, London, pp 57–147

    Google Scholar 

  • Ramirez JM, Pearson KG (1988) Generation of motor patterns of walking and flight in motoneurons supplying bifunctional muscles in the locust. J Neurobiol 19: 257–282

    Google Scholar 

  • Settles HE, Hanken J, Bekoff A (1987) Functional compartments of the chick iliofibularis (biceps) muscle. Am Zool 27: 23A

  • Smith JL (1986) Hindlimb locomotion in the spinal cat: synergistic patterns, limb dynamics and novel blends. In: Grillner S, Stein PSG, Stuart DG, Forssberg H, Herman RM (eds) Neurobiology of vertebrate locomotion. Macmillian, Hampshire, England, pp 185–199

    Google Scholar 

  • Smith JL, Hoy MG, Koshland GF, Phillips DM, Zernicke RF (1985) Intralimb coordination of the paw-shake response: a novel mixed synergy. J Neurophysiol 54: 1271–1281

    Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. W.H. Freeman, New York

    Google Scholar 

  • Stein PSG, Currie SN (1989) Motor program selection in the vertebrate spinal cord: three forms of the scratch reflex in the turtle. In: Erber J, Menzel R, Pflüger H-J, Todt D (eds) Neural mechanisms of behavior: Proceedings of the Second International Congress of Neuroethology. Georg Thieme, Stuttgart, pp 178–179

    Google Scholar 

  • Stein PSG, Mortin LI, Robertson GA (1986) The forms of a task and their blends. In: Grillner S, Stein PSG, Stuart DG, Forssberg H, Herman RM (eds) Neurobiology of vertebrate locomotion. Macmillian, Hampshire, England, pp 185–19

    Google Scholar 

  • Systat (1992) SYSTAT: Statistics, Version 5.2 Edition. SYSTAT, Evanston, IL

    Google Scholar 

  • van Ingen Schenau GJ (1987) The unique action of bi-articular muscles in complex movements. J Anat 155: 1–5

    Google Scholar 

  • van Ingen Schenau GJ (1990) On the action of biarticular muscles, a review. Neth J Zool 40: 521–540

    Google Scholar 

  • van Ingen Schenau GJ, Boots PJM, de Groot G, Snackers RJ, van Woensel WWLM (1992) The constrained control of force and position in multi-joint movements. Neuroscience 46: 197–207

    Google Scholar 

  • Weeks JC, Levine RB (1990) Postembryonic neuronal plasticity and its hormonal control during insect metamorphosis. Annu Rev Neurosci 13: 183–194

    Google Scholar 

  • Weimann JM, Meyrand P, Marder E (1991) Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J Neurophysiol 65: 111–122

    Google Scholar 

  • Williams TL (1981) Experimental analysis of the gait and frequency of locomotion in the tortoise, with a simple mathematical description. J Physiol (Lond) 310: 307–320

    Google Scholar 

  • Young JZ (1981) The life of vertebrates. Third edition. Oxford New York, pp 327–334

    Google Scholar 

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Author notes

  1. R. M. Johnston

    Present address: ARL — Division of Neurobiology, University of Arizona, 85721, Tucson, AZ, USA

Authors and Affiliations

  1. Department of Environmental, Population and Organismic Biology and The Center for Neuroscience, University of Colorado, 80309-0334, Boulder, CO, USA

    R. M. Johnston & A. Bekoff

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  2. A. Bekoff
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Johnston, R.M., Bekoff, A. Patterns of muscle activity during different behaviors in chicks: implications for neural control. J Comp Physiol A 179, 169–184 (1996). https://doi.org/10.1007/BF00222784

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